Male and female fruitflies use pheromones to flaunt their species identity and gender as they court amid other fruitfly species. The grammar of this chemical language is surprisingly sophisticated.
Successful mating is all about making the right choices. But, as we all know, this is not an easy undertaking. Before engaging in courtship, a male needs to make sure that a potential mate is actually female, that she is of the same species, and is sexually mature and receptive. Meanwhile, in addition to checking species and gender, a female needs to assess her suitor's qualities before she accepts him as a mate. Therefore, although males often make the first move by deciding whom to court, females have the last word in deciding with whom they will mate. The primary signals that animals use to guide these decisions are sensory inputs, but it is largely unclear how such signals translate into stereotyped behavioural decisions. On page 987 of this issue, Billeter and colleagues1 shed light on this matter by deciphering the chemical dialogue that takes place between male and female fruitflies as they vie for success in the mating game.
The fruitfly Drosophila melanogaster mates at dinner, which typically takes place in a compost heap. The trouble is that this dining area is abuzz with many different fruitfly species, which often look remarkably similar. How can a male distinguish a female of the same species among the crowd? Chemical communication in the form of pheromones seems to constitute the key signal2,3. Pheromones are compounds that are exchanged between prospective mates by means of olfaction or gustation before and during mating4,5. They have long been known to have a central role in mate choice and the decision to mate in various animals, from insects to mammals. But the precise role of individual pheromones in sexual communication has been difficult to assess because pheromones are usually secreted as blends6 (about 30 different molecules cover the fly body), and they function in conjunction with other signals.
Billeter et al.1 tackled this problem by assessing the function of individual pheromones one at a time using a simple but powerful approach. First, they engineered D. melanogaster flies that are devoid of any pheromone by using genetic tools to deplete the cells that secrete these molecules. Then they perfumed these chemically mute flies with individual pheromones or blends of pheromones, and tested the effects on other flies.
To their surprise, unlike Patrick Süskind's odourless protagonist Jean-Baptiste Grenouille in the novel Perfume, the unscented flies, regardless of their gender, are hyperattractive to males. This result contradicts the widespread belief that pheromones are required to initiate courtship3 and suggests that other sensory inputs such as vision may be a trigger for mating. Moreover, when perfumed with the female D. melanogaster pheromone 7,11-HD, long thought to be an aphrodisiac, the scentless flies do not become any more appealing to males — as the authors reveal, the aphrodisiac role of 7,11-HD is more subtle than previously thought.
During copulation, a male-specific chemical compound, cVA, is transferred to the female. This pheromone modifies the female's post-copulatory behaviour — for instance, by inducing egg-laying — and deters other suitors7. Billeter et al. show that, as expected, the sex appeal of odourless flies perfumed with cVA decreases. Surprisingly, however, they find that the addition of 7,11-HD on top of cVA lowers the deterrent effect of cVA in a dose-dependent manner. Hence, a female compound, 7,11-HD, can counter the chemical chastity belt imposed by cVA and broadcast a female's receptivity. This pheromonal negotiation illustrates the conflicting agendas of sexual partners: it is in the male's interest that his conquest doesn't re-mate with another male, whereas the female seeks to maximize the chances of having her eggs fertilized by mating with several different males.
Now, what happens when a male of species A approaches a female of species B? Odourless flies elicit courtship from males of different species, indicating that pheromones impart species identity. Billeter et al.1 show that, although 7,11-HD attracts D. melanogaster males, it deters males of other species whose female members do not secrete 7,11-HD, and is sufficient to discriminate between different species (Fig. 1). Therefore, a single fly pheromone has a central role in mate choice by tagging both female and species identity.
By studying the effect of single pheromones, Billeter and colleagues reveal the unexpectedly subtle and complex nature of the chemical dialogue that takes place between sexual partners, and lay the groundwork to address related questions. Flies, like other animals, receive countless sensory signals that are integrated to generate appropriate behaviours. How this integration is computed in the brain is still a mystery. The neural integration of different pheromones is illustrated by the opposite effects of 7,11-HD and cVA. When exposed to both compounds at the same time, a fly has to decide what to do — whether to exhibit one behaviour (courting) or another (not courting). Where and how does this integration happen in the brain? The receptor for cVA has been identified8,9, as have aspects of the neuronal pathway that mediates its response10. However, for 7,11-HD, neither its receptor nor the neuronal circuitry transducing its effects is known — this information is a prerequisite for understanding the neural basis of pheromone-signal integration.
The authors' work1 also touches on how the chemical dialogue of courtship evolves by changes in both signal emission (the pheromones) and signal reception (the neuronal circuit processing the signal). Although it is well documented that the composition of the pheromone bouquet evolves quickly among species4,5, little is known about the evolution of the perception of these chemical cues. What is the difference between D. melanogaster males that are attracted by 7,11-HD and their kin from other species that are deterred by the same compound? Are these distinctions located in sensory neurons — for example, does 7,11-HD bind different receptors in different species, triggering divergent responses? Or are disparities in pheromone perception due to processes lodged more deeply in the brain's circuitry? The difference among fruitfly species parallels that of male and female D. melanogaster, which respond differently to cVA. In this case, the sexually dimorphic response is known to lie deeper in the neuronal circuit, in the form of subtle differences in synapse morphology10.
Billeter et al.1 have taken a crucial step in dissecting pheromonal inputs to courtship initiation in the fruitfly. But how sensory representation leads to decision-making, and the evolution of this representation among species, awaits further study.
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